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Reef Corals : Autotrophs Or Heterotrophs?

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Reference : Biol. Bull., 141 : 247—260. (October, 1971) REEF CORALS : AUTOTROPHS OR HETEROTROPHS? THOMAS F. GOREAU,1 NORA I. GOREAU AND C. M. YONGE Discovery Bay Marine Laboratory, Department of Zoology, University of the West mndies, Mona, Kingston 7, Jamaica; and Department of Zoology, University of Edinburgh, Edinburgh, Scotland Some recent studies 2 seem to indicate that the nutritional economy of reef corals is for all practical purposes to be considered autotrophic due to their zooxanthellae (Fig. 1). For example, Franzisket (1969a, 1970) claims to have demonstrated that some Hawaiian reef corals can achieve net growth in the total absence of particulate food, while Johannes and Coles ( 1969) state that the energy requirements of Bermudian reef corals are in some cases more than an order of magnitude greater than could be provided by the zooplankton which the investi gators were able to catch with a fine net. In spite of their supposedly autotrophic economy, the reef corals have not developed any of the behavioral and structural specializations for such a way of life. In this respect they differ fundamentally from Xenia hicksoni and Clavularia hanira (Octocorallia, Alcyonacea) (Gohar, 1940, 1948) and Zoanthus sociatus (Hexacorallia, Zoanthidea) (Von Holt and Von Holt, 1968a, b) , unrelated anthozoans which have independently evolved a more or less complete nutritional dependence upon their contained zooxanthellae. Available data is summarized in Table I. These species have never been observed to feed, and there is a more or less marked reduction of structures and functions associated with the usual predatory feeding habits in Cnidaria ; for example, they do not respond to any of the known tactile and chemical stimuli that trigger feeding behavior in related carnivorous species; they do not ingest particulate matter, and are unable to either digest or assimilate food artificially placed into their coelenteron by means of a canula (Goreau and Goreau, unpublished). The reef corals are, by contrast, superbly efficient and voracious carnivores that will accept practically any kind of particulate animal food (Yonge, 1930a, 1930b; Yonge and Nicholls 1930, 1931). Feeding occurs in several different ways, de pending on the species: in the majority, the food is swept into the coelenteron by means of ciliary currents, (sometimes involving reversal as in Fungia), while in some corals the tentacles convey the food directly to the mouth (Yonge, 1930a). Most species are also capable of extracoelenteric digestion of food matter outside the body by means of mesenterial filaments extruded through temporary openings (Fig. 2) at any place on the colony surface (Duerden, 1902; Matthai, 1918; Goreau, 1956). Reef corals obtain food via this ancillary route and also use the extruded filaments as weapons, primarily against other corals the tissues of which they may digest (Lang, 1969, 1970). 1 Thomas F. Goreau was Professor of Marine Sciences, University of the West Indies at Mona, and Professor of Biology, State University of New York at Stony Brook; Director of the Coral Reef Project and Director of the Marine Laboratory at Discovery Bay, Jamaica. He died unexpectedly in New York on April 22, 1970. 2 See also the paper by V. B. Pearse and L. Muscatine (dedicated to the late T. F. Goreau) on pages 350—363,and that by P. V. Fankboner on pages 222—234of this issue—Editor. 247 248 THOMAS F. GOREAU, NORA I. GOREAU AND C. M. YONGE FIGuu.@ 1. Autoradiogran1 of carbon1' labelled Fungia scutaria. The coral was ex posed to ‘¿4C02in sunlight for ten minutes and washed in running sea water for thirty minutes before fixation. The area seen under (lark field illumination and focused on the plane of emul sion shows the concentration of silver grains over the carbon― labelled zooxanthellac of the gastrodermis. The scale represents 100 @. Specimens exposed in the (lark showed no fixation of the isotope. FIGURE 2. Mussa angulosa under severe starvation gradually loses contact with the skele ton (a) (b), eventually sinking to the bottom of the aquarium, still alive. When offered crab juice this free specimen extruded its mesenterial filaments (c) through the epithelium of the calicoblast. Some colonies lose their zooxanthellae, some keel) them, but in the most severe cases of starvation only the stoniodeum and a few filaments remain. Later only bits of mesenterial filaments curl about. However they all showed feeding responses when crab meat or amino acids were added. These filaments persist for a few (lays. These diverse feeding mechanisms are supplemented by an exquisitely per ceptive chemotactic sense. In several species of Jamaican reef corals (Manicina areolata, Cladocora arbuscula, Eusnülia fastigiata, Isophvllia sinuosa., Mussa angulosa and Scolvm.ia lacera) we found some years ago that very low concen trations of amino acids such as glycine, alanine. phenvlalanine and lucine could trigger off typical feeding responses; i.e., opening and eversion of the stomodeum, swelling of the coenosarc, extension of tentacles and sometimes extrusion of mesenterial filaments. M. areolata responded in this manner to alanine and glvcine at concentrations as low as 10@ @i,whereas glucose, sucrose, glycerol and mannitol did not have any effect at high concentrations. Mariscal and Lenhoff (1968) ob TROPHIC CONDITIONS OF REEF CORALS 249 TABLE I Available data on nutritional adaptation and absorption in Scleraclinia, Alcyonacea and Zoanthidea of of of re crab juice ‘¿Hleucine sponse to TaxonomyZooxanthellaeAbsorption and india ink into the C by crab meat or acidsNematocystsScieractinia: into filamentsUptakeepidermisUptakezooxantliellaeFeedingamino Hermatypes: Fungia + Stylophora + +++ +++ ++ +++ +++ Ahermatype: Tubastrea 0 +++ +++ 0 +++ +++ Alcyonacea: Xenia + 0 ? +++ 0 0 Zoanthidea: Z. sociatus + ? ? +++ ? disordered P.caribbae + +++ ? + +++ ++ P. grandis ++++ ++++++ ?++ ++++ ++++++ ++ Other niorphological correllates with xanthellar symbiosis are: (1) Xenia: nonematocysts,reducedfilaments,noseptallobes, (2) Zoanthus: nematocysts,butthesearein a disorderedpositionandin placeswheretheydonogood; filaments reduced but lobesare very large. All stages of pycnosis, degeneration,frag mentation and extrusion of zooxanthellae were observed in the mesenterial lobes. Feeding reaction: (1) Corals: Dilationand extensionof stomodeum,inibibitionof water,sometimeserectionof tentacles or shooting of the mesenteries through mouth or body wall; (2) Xeniids: Rhythmic movement of tentacles of anthocodia; (3) Zoanthids:Zoanthussociatus:none, Palythoa caribbae : Dilation of mouth, strongly inward movement of water at ciliate groove, curling over of the lenkicular rinz, Palythoa grandis: same as P. caribbae. served tilat concentrations as low as 10@ M proline resulted in feeding responses in C@'plzastrea ocellina., Pocillopora dai'nicornis and Fungia scutaria. Responses similar to tilose caused by amino acids are produced in corals by seawater ill which there had previously been zooplankton. We have often observed that corals will expand tinder llattlral conditions in apparent anticipation of plank ton: evidently this is due to tileir ability to sense the diffuse cloud of metabolites, including amino acids, that usually surrounds plankton swarms (Hellebust, 1965). It would indeed be surprising if, as Johannes and Coles (1969) have speculated, tilecoralshave retainedtllesecapabilitiesmerely to obtaintracenutrientssuch as phosphorus from their prey while the bulk of their nutrition comes from the zooxantheilae! Yet, there is no need for such a roundabout way to obtain phos phorus since reef corals, but not ahermatypes, in the light are known to take up inorganic phosphate from the mediunl, this being a function of the zooxantheilae, not the coral host (Yonge alld Nidllolls, 1931). The fully autotrophic xeniid alcyonaceans and Zoanthus are evidently able to obtain all their trace nutrients directly from tile seawater. As regards the possible need for organic phosphorus, Von Holt (1968) has shown that ill Zoanthus there is a transfer of nucleoside polyphospilate fronl algal symbiont to animal host. If the reef corals were truly 250 THOMAS F. GOREAU, NORA I. GOREAU AND C. M. YONGE as autotrophic as Franzisket and Johannes believe, the question arises why have they not evolved similar more direct mechanisms for obtaining critical nutrients directly from their symbionts? OBSERVATIONS The boundary layer water and its relation to the trophic structure of the reef The evidence so far cited has not resolved the conflict between the apparent low productivity of tropical ocean surface waters (Fleming, 1954 ; Sargent and Austin, 1949, 1954) and the need for organic nutrients by the benthonic fauna in the reef ecosystem. This consists of the corals and a diverse assenlblage of filter, detritus, suspension and deposit feeders as well as predacious carnivores, the ma jority without zooxanthellae which might serve as ancillary food source. Recent reviews by Bakus ( 1969) and Stoddart ( 1969) have demonstrated how little quantitative information is available on the trophic cycles within the reef bio tope, largely because the pathways themselves are still largely unknown. Oceanic reef ecosystems appear on the whole to be autotrophic units operating at very high levels of productivity, turnover rate and efficiency (Odum and Odum, 1955; Kohn and Helfrich, 1957) whereas at least sonie smaller reefs off high islands may be non-autotrophic (Goreau, Torres, Mas and Ramos, 1960 ; Gorden and Kelley, 1962)
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  • Cnidarian Phylogenetic Relationships As Revealed by Mitogenomics Ehsan Kayal1,2*, Béatrice Roure3, Hervé Philippe3, Allen G Collins4 and Dennis V Lavrov1

    Cnidarian Phylogenetic Relationships As Revealed by Mitogenomics Ehsan Kayal1,2*, Béatrice Roure3, Hervé Philippe3, Allen G Collins4 and Dennis V Lavrov1

    Kayal et al. BMC Evolutionary Biology 2013, 13:5 http://www.biomedcentral.com/1471-2148/13/5 RESEARCH ARTICLE Open Access Cnidarian phylogenetic relationships as revealed by mitogenomics Ehsan Kayal1,2*, Béatrice Roure3, Hervé Philippe3, Allen G Collins4 and Dennis V Lavrov1 Abstract Background: Cnidaria (corals, sea anemones, hydroids, jellyfish) is a phylum of relatively simple aquatic animals characterized by the presence of the cnidocyst: a cell containing a giant capsular organelle with an eversible tubule (cnida). Species within Cnidaria have life cycles that involve one or both of the two distinct body forms, a typically benthic polyp, which may or may not be colonial, and a typically pelagic mostly solitary medusa. The currently accepted taxonomic scheme subdivides Cnidaria into two main assemblages: Anthozoa (Hexacorallia + Octocorallia) – cnidarians with a reproductive polyp and the absence of a medusa stage – and Medusozoa (Cubozoa, Hydrozoa, Scyphozoa, Staurozoa) – cnidarians that usually possess a reproductive medusa stage. Hypothesized relationships among these taxa greatly impact interpretations of cnidarian character evolution. Results: We expanded the sampling of cnidarian mitochondrial genomes, particularly from Medusozoa, to reevaluate phylogenetic relationships within Cnidaria. Our phylogenetic analyses based on a mitochogenomic dataset support many prior hypotheses, including monophyly of Hexacorallia, Octocorallia, Medusozoa, Cubozoa, Staurozoa, Hydrozoa, Carybdeida, Chirodropida, and Hydroidolina, but reject the monophyly of Anthozoa, indicating that the Octocorallia + Medusozoa relationship is not the result of sampling bias, as proposed earlier. Further, our analyses contradict Scyphozoa [Discomedusae + Coronatae], Acraspeda [Cubozoa + Scyphozoa], as well as the hypothesis that Staurozoa is the sister group to all the other medusozoans. Conclusions: Cnidarian mitochondrial genomic data contain phylogenetic signal informative for understanding the evolutionary history of this phylum.